Introduction
Interoception describes the perception and integration of autonomic, hormonal, and homeostatic signals that collectively represent the physiological state of the body (Barrett and Simmons
2015), through the continuous dynamic feedback of afferent visceral signals to the brain (Critchley and Harrison
2013).The personal accounts of autistic individuals and their caregivers suggest a range of pervasive difficulties with the awareness and integration of interoceptive signals (Elwin et al.
2012; Gerland
1997; Musser
2018). Many of these accounts document a lack of awareness of hunger, thirst, pain and the need to make bowel or bladder movements. Difficulties with distinguishing between emotional and interoceptive states are also described (Musser
2018). Within the last few years, direct empirical investigations of interoceptive processing have emerged, which generally support the idea that interoception is atypical in autism (see DuBois et al.
2016, for review, although see Nicholson et al.
2018, Schauder et al.
2015, and Shah et al.
2016, for reports of intact interoception).
Recently, Garfinkel and colleagues proposed a three-dimensional construct of interoception (Garfinkel and Critchley
2013; Garfinkel et al.
2015). Within this model, paradigms that objectively quantify participants’ performance in detecting internal events represent measures of ‘interoceptive accuracy’ (Garfinkel et al.
2015). Questionnaire based self-report measures, and confidence judgements on objective tasks, are thought to quantify an individual’s subjective awareness of interoceptive signals and are termed ‘interoceptive sensibility’. Finally, the trial-wise correspondence between performance and confidence on objective tasks, referred to as ‘interoceptive awareness’, is thought to reflect an individual’s metacognitive insight into their interoceptive ability. This framework outlined how individuals could diverge on subjective and objective measures of interoceptive functioning.
To date, only a few studies have simultaneously considered multiple interoceptive dimensions in autism (Garfinkel et al.
2016; Mul et al.
2018; Palser et al.
2018a). In the main, these studies suggest reduced objective interoceptive accuracy with concomitant heightened interoceptive sensibility in autistic adults
and children. Of note, when more mindfulness-related measures of interoceptive sensibility that focus on the effective interpretation of interoceptive signals are employed, such as the Multidimensional Assessment of Interoceptive Awareness (MAIA, Mehling et al.
2012), reduced interoceptive sensibility has been reported (Mul et al.
2018). As such, interoceptive sensibility in autism likely varies according to the measure employed. Presently, these questionnaires are all considered to represent the construct of interoceptive sensibility, but in the future it is conceivable that a dissociation will be argued for.
Garfinkel and colleagues further conceptualized the difference between interoceptive accuracy and sensibility as an interoceptive trait prediction error (ITPE), which provides a measure of whether an individual tends to overestimate or underestimate their interoceptive abilities (Garfinkel et al.
2016). Autistic adults and children have been found to differ significantly from non-autistic participants on this measure, indicating a tendency towards overestimation of their interoceptive abilities (Garfinkel et al.
2016; Palser et al.
2018a). Moreover, this measure predicts the severity of anxiety symptoms, with the most severe anxiety seen in those who most overestimate their interoceptive abilities. These findings suggest a divergence in how interoceptive dimensions relate to the co-occurring features of autism, emphasising the potential importance of considering interoceptive functioning on multiple measures.
The finding of interoceptive differences in autistic people does not always replicate (Nicholson et al.
2018; Schauder et al.
2015; Shah et al.
2016). Some researchers have suggested a divergent developmental trend in autism (Mash et al.
2017; Nicholson et al.
2019), such that differences present early in development may abate by adulthood (Nicholson et al.
2019) or that the effect of age on interoception may be moderated by cognitive ability, with a reduction in interoceptive accuracy with age in autistic children with an IQ under 115 (Mash et al.
2017). However, as yet, no longitudinal studies have been conducted on interoception in autism and it is possible that cohort effects may be driving cross-sectional observations.
Analysis protocols also likely differ between testing sites. For example, some researchers might exclude participants who cannot detect any heartbeats (e.g., Schauder et al.
2015), thereby discarding the participants with the poorest awareness of their interoceptive signals. A further possible explanation for the mixed results to date is differences in sampling characteristics between study populations—including the severity of autism-related symptoms. It is possible that those with more severe autistic features also show more severe interoceptive difficulties. Preliminary support for this possibility comes from work in neurotypical adults, which show an association between interoceptive processing and some of the core areas of cognition affected in autism, for example, a positive correlation between interoceptive accuracy and emotional theory of mind abilities (Shah et al.
2017).
Only three studies to date have adopted such an individual differences approach, with inconclusive results (Mul et al.
2018; Palser et al.
2018a; Shah et al.
2016). One study found no relationship between interoceptive accuracy and autistic traits as measured with the Autism Quotient (AQ; Baron-Cohen et al.
2001) in both non-autistic and autistic adults (Shah et al.
2016). A second found that the Awareness dimension of the Multidimensional Assessment of Interoceptive Awareness (MAIA) (comprising trusting, noticing and emotional awareness) related negatively to autistic traits on the AQ (Mul et al.
2018). Yet, the AQ has been criticized for being a poor predictor of clinically-assessed signs of autism (Ashwood et al.
2016) and therefore might not be the best measure for such an analysis. In a third study, we reported a weak negative relationship between standardized severity scores on the gold-standard Autism Diagnostic Observation Schedule (ADOS-2; Lord et al.
2012) and interoceptive sensibility and a stronger negative relationship with ITPE in a sample of 30 autistic children and adolescents (Palser et al.
2018a). No relationship, however, was found between autism severity and interoceptive accuracy.
It is also possible that interoceptive processing might vary in how it relates to the aspects of autism, such as emotion. Indeed, it has been argued that the higher rates of interoceptive differences observed in autism actually reflect higher rates of emotional difficulties in the condition, termed ‘alexithymia’, rather than autism per se (Gaigg et al.
2018; Shah et al.
2016). The salient features of alexithymia are difficulties in identifying and describing feelings, in distinguishing between feelings and bodily sensations of emotional arousal, in imagination, and an externally-oriented cognitive style (Nemiah et al.
1976). Alexithymia in autism has been found to be associated with reduced interoceptive accuracy (Shah et al.
2016), although recent null findings call this link into question (Mul et al.
2018; Nicholson et al.
2018).
The relationship between interoceptive sensibility and alexithymia appears to vary according to the measure employed. When more mindfulness-related measures of interoceptive sensibility are used, with a focus on the effective interpretation of interoceptive signals, interoceptive sensibility has been shown to be negatively correlated with alexithymia (Mul et al.
2018). Other measures of interoceptive sensibility that tap a more vigilant, anxiety-associated style have a positive relationship with alexithymia (Longarzo et al.
2015; Palser et al.
2018b), although this has yet to be replicated in an autistic population. It is possible that interoceptive differences vary according to the extent of autistic individuals’ socio-emotional difficulties. It may therefore be important to consider how interoceptive processing relates not only to overall autism severity, but also to the severity of specific features, particularly social and affective domains.
In sum, previous studies suggest that altered interoception is more likely, but not always, seen in autism than the general population, and is related to some of the co-occurring features of the disorder, namely anxiety. Yet, it is still unknown how interoceptive processing relates to the core features of the condition, including the social affective and restricted and repetitive behavior domains. Here, we used the ADOS-2 (Lord et al.
2012) to examine the relationship between interoceptive dimensions (interoceptive accuracy, interoceptive sensibility, ITPE) and autism severity. Specifically, we hypothesized that calibrated severity scores on the ADOS-2 would be (a) negatively related to interoceptive accuracy scores, such that lower interoceptive accuracy should be seen in those with greater autism severity, and (b) positively related to interoceptive sensibility, such that those with greater autism severity should report the highest beliefs about their interoceptive ability (operationalized by subjective ratings of awareness and confidence on heartbeat detection tasks). In turn (c) these differences should result in a positive relationship between autism severity scores and ITPE, with the greatest mismatch between ability and belief in those with the most severe features. Additionally, based on evidence that social and affective performance is linked to interoception (e.g., Shah et al.
2017), and at present, a lack of evidence of a link between repetitive restricted behaviors and interoception, we hypothesized that interoceptive differences should relate more strongly to the symptom dimension of social affect (SA), than restricted and repetitive behaviors (RRB).
Discussion
In this study, we hypothesized that there would be a relationship between core autism features and interoceptive differences in autism. Specifically, we predicted that we would observe decreasing interoceptive accuracy but increasing interoceptive sensibility as autism severity increased. This would result in a positive association between interoceptive trait prediction error (ITPE)—the discrepancy between interoceptive accuracy and interoceptive sensibility—and core autistic features, especially in the social affective (SA) domain.
In partial support of our hypotheses, the results indicated that there was a positive association between autism severity, as measured using calibrated severity scores from the ADOS-2 (Lord et al.
2012) and interoceptive differences in the domain of interoceptive sensibility. Higher judgements of confidence on the heartbeat discrimination task were linked to greater autism severity. As predicted, this finding was driven by features in the SA domain; when domains were separated, the association was replicated in this but not the RRB domain. Counter to our hypotheses, interoceptive accuracy on the heartbeat discrimination task related positively to symptoms in the RRB domain. Furthermore, and also inconsistent with our hypotheses, there was a weakly significant negative correlation between confidence on the heartbeat tracking task and overall autism severity. These findings suggest that the different autism feature clusters might diverge in their relationships to distinct aspects of interoceptive processing.
Inflated confidence in interoceptive judgements on the heartbeat discrimination task was associated with greater SA severity. Heightened interoceptive sensibility has previously been linked to alexithymia, a difficulty with reasoning about one’s own affective state (Mul et al.
2018), and anxiety (Palser et al.
2018b). Previously, a combination of high confidence in interoceptive ability and poor performance has been observed in autistic participants (Garfinkel et al.
2016; Palser et al.
2018a). In addition, we also observed evidence that low confidence in interoceptive judgements on a different task was associated with greater symptom severity. Taken together, these findings suggest that subjective confidence might represent a noisier channel of information, at least in children on the autism spectrum, with a difficulty mapping belief to performance.
Autism has previously been framed as a ‘disorder of metacognition’, resulting from altered beliefs about the reliability of sensory inferences (Lawson et al.
2014). This might reflect a reduced influence of prior experience on current estimations (Pellicano and Burr
2012) or inflexible predictions about current states (Van de Cruys et al.
2013). Reduced insight into one’s access to interoceptive states may be linked to a reduced ability to infer these states in others. It has previously been suggested that similar systems may support both the ability to self-reflect and infer the thoughts, beliefs and behaviors of others (Carruthers
2009, Frith and Frith
2001; Frith and Happé
1999; Mitchell et al.
2005). As such, good metacognitive insight, including interoceptive insight, may scaffold the development of social competencies, particularly the ability to mentalize about others. The finding of an association between interoceptive confidence judgements and autism features, in combination with the lack of association to interoceptive accuracy, which is thought to measure an individual’s (conscious) access to these signals, suggests it may be the confidence placed in the detection of that interoceptive signal and not the detection of the interoceptive signal itself that is of most importance to many of the core features of autism.
Unfortunately, we were not able to calculate scores for interoceptive awareness, the third dimension in Garfinkel and colleagues’ interoception model. Such analyses generally require the calculation of the area under the receiver operating characteristic (ROC) curve, which quantifies in one value, how well confidence follows accuracy. These methods originated in the exteroceptive perceptual metacognition literature where they were most often applied to visual perception tasks (e.g. Fleming et al.
2010). Extending the confidence scale to sufficient extent that robust calculation of ROC curves would have been possible was judged to be too complicated for younger participants. Only one study to date has measured interoceptive awareness in autistic participants, and found no significant differences in adults diagnosed with the condition, relative to neurotypical adults (Garfinkel et al.
2016). Nonetheless, further work should seek to examine if individual differences in this interoceptive dimension relate specifically to social and affective understanding.
The positive relationship between interoceptive accuracy and RRB symptoms is curious, and, at first glance, counter to previous findings of reduced interoceptive accuracy in autism (Garfinkel et al.
2016; Mul et al.
2018; Nicholson et al.
2019; Palser et al.
2018a). Both high performance on the heartbeat tracking task and engagement in RRBs require highly focused attention while ignoring external distractors. It is possible that the children who are most attentive in this manner, due to elevated RRBs, also represent those most capable of focussing their attention on cardiac signals when instructed. RRBs are often thought of as maladaptive, distracting the child from social engagement or learning. However, there is evidence to suggest that some of the RRBs in which autistic children frequently engage, such as hand flapping and body rocking, are self-soothing and may have an adaptive function as a means of lowering arousal and regulating the autonomic nervous system (which generates interoceptive signals) (Hutt et al.
1975; Kapp et al.
2019).
RRB features were only predicted by interoceptive accuracy on the heartbeat discrimination task, not the heartbeat tracking task. Previously, the latter has been the most sensitive measure of interoceptive accuracy differences in autistic people (Garfinkel et al.
2016; Mul et al.
2018; Palser et al.
2018a). However, there has recently been increasing criticism of the heartbeat tracking task due to the necessity of multiple control measures and its relatively poor psychophysical properties (Murphy et al.
2018; Zamariola et al.
2018). These concerns may explain the variability in this measure across studies. There are also limitations associated with the heartbeat discrimination task. This task may not be a pure interoceptive measure, as it requires the temporal integration of an interoceptive signal (the heartbeat) with an exteroceptive signal (the tone). Differences in multisensory integration have been well-documented in autism (e.g., Brandwein et al.
2015) and, as such, it is interesting that no group differences have yet been observed on this measure.
Much like the broader literature on interoception, studies of interoceptive processing in autism have almost exclusively focussed on cardiac interoception. Many of the reasons for this focus are pragmatic. The heartbeat represents a discrete regular event that is easily and non-invasively recorded. Most individuals experience at least some conscious awareness of the signal and can easily compare detected versus occurred events. Aside from these practical issues, the popularity of heartbeat detection paradigms rests in part on the assumption that interoceptive accuracy represents an overall or general interoceptive capacity. This assumption may mask important differences in autism between sources of interoceptive information. While in the cardiac domain, autistic individuals are more likely to experience reduced awareness, an aversion to social touch is frequently seen in infants who later obtain an autism diagnosis, suggesting heightened perception in this domain (Baranek
1999; Grandin and Scariano
1986). Interoceptive functioning should now be assessed in autism using other measures, such as tests of water load and taste sensitivity (Murphy et al.
2018; Van Dyck et al.
2016) to assess if the present findings of an association between cardiac interoception and core autism features generalize to other interoceptive systems.
Some authors argue that any interoceptive differences seen in autism are in fact the result of high levels of comorbid alexithymia, rather than autism itself (Gaigg et al.
2018; Shah et al.
2016). Studies indicate that around 50% of autistic people also show clinically meaningful levels of alexithymia (Griffin et al.
2016; Hill et al.
2004). As alexithymia involves the individual’s experience of their own emotions, in the vast majority of cases it is measured using a self-report questionnaire. Accurate completion of such a measure therefore requires sufficient insight on the part of the participant. That is, they must be aware that they are experiencing difficulties with their emotions, and that other people’s experiences are different, in order to report such difficulties. The validity of such measures in children, particularly autistic children, is unclear. The only study to have used an alexithymia measure with children yielded no significant correlation between parent- and child-rated alexithymia in this population (Griffin et al.
2016). For this reason, a measure of alexithymia was not included in the current study. That being said, some of the emotional presses in the ADOS-2 appear to tap alexithymic difficulties, by testing how well the participant describes the experience of several emotions. Some recent investigations have failed to show a relationship between alexithymia and interoceptive differences in autistic people (Nicholson et al.
2018,
2019) and the present study demonstrates a link between the non-emotional features of autism (RRBs) and interoception, suggesting alexithymia may not explain the entirety of interoceptive differences in autism. Nevertheless, the absence of measures of alexithymia and anxiety in the current study, which have been previously found to be associated with interoception in autism, are potential limitations of the current study. Future work should seek to explore this question further, with the development of validated measures of alexithymia in autistic child populations.
Some further limitations of the study are discussed below. Interoception only explained a small amount of the variance in symptom severity, Indeed, the sex of participants explained more variance at both the level of overall symptoms and in the SA domain. Each symptom domain reflects a broad range of behaviors, and is likely shaped by multiple biological, psychological and situational factors. Given such a diverse set of antecedents, any one factor, at any particular level of analysis, will likely explain only a fraction of an individual’s autistic features. The present findings suggest that interoceptive processing may represent one psychological antecedent, although further work is now needed to establish a causal link. Indeed, theoretical accounts that posit a role for atypical interoception in autism are causal models, explicitly relating interoception to the development of autism (Quattrocki and Friston
2014). The correlational data presented here, while consistent with the predictions of these hypotheses, do not offer sufficient evidence to support such a causal claim. Longitudinal research beginning early on in development, and the manipulation of interoceptive processing while observing the effect on autistic features, will be necessary to further our understanding of the relationship between autism and interoception.
Taken together, the current findings extend existing findings showing a link between interoception and the co-occurring features of autism (namely anxiety), to the core features of the condition, in both the domains of social and affective processing and repetitive and restricted behaviors. However, these domains relate to distinct aspects of interoceptive processing suggesting that considering autism severity as a single dimension may mask important relationships between autistic features and interoception. If replicated, the divergence between how distinct symptom clusters relate to different domains of interoceptive processing suggests that we may need to tailor interventions to individual interoception-symptom profiles.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.